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Persulfidation in plants: the new phosphorylation?

In Journal of Experimental Botany: One in 20 proteins in Arabidopsis is persulfidated: this we now know. Evidence of the role played by hydrogen sulfide signalling in plants has been building in recent years, and it is new methodology which has revealed the likely extent. Indeed, the study by Angeles Aroca and colleagues in Journal of Experimental Botany goes further in showing an association with a wide range of biological functions. See also the separate Insight article for further reflection on the implications of this ground-breaking research, including the questions it opens up from our knowledge of animal systems.

Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis.

More than just an intermediate: hydrogen sulfide signalling in plants

Rotten eggs and air pollution were, until quite recently, most people’s first and last thoughts on hydrogen sulfide (H2S). But research in animals and then plants has been ripping the lid on its role in signalling over the past decade. Despite this, there have been question marks against some of the methodology for identifying persulfidated proteins, and a new technique has been sought. The tag-switch method, described in 2014 by Zhang et al., is the answer. In the first step of this technique methylsulfonylbenzothiazole (MSBT) is used to block both thiol and persulfide groups; after this, the activated disulphide reacts to a tag-bearing nucleophile (CN-biotin).

The whole persulfidome

Aroca et al. looked at the whole Arabidopsis persulfidome, a significant undertaking but one which will be immensely valuable for the field. Over 2000 persulfidated proteins were identified in wild-type plants. The authors also looked at L-CYSTEINE DESULFHYDRASE 1 (DES1) mutants – the DES1 enzyme is critical for cytosolic sulfide production needed for signalling. Although only 47 proteins were down-persulfidated compared with the control, specific targets included protein kinases, phosphatases and defence response molecules.

Aroca et al.: ‘The 2015 persulfidated proteins identified in wild-type plants represent at least 5% of the entire proteome of 35 386 proteins encoded by the Arabidopsis thaliana genome … Moreover, our proteomics analysis was performed on plants grown under physiological conditions and the magnitude of this modification may be even higher under conditions where sulfide has been demonstrated to play a signaling role, such as plant responses to a variety of plant stresses, autophagy, stomatal movement and photosynthesis.’

Considering the implications of the work in an Insight article, Milos Filipovic and Vladimir Jovanovic draw from animal physiology, noting the importance, for example, of understanding links with another gasotransmitter, nitric oxide (NO); and from use of persulfidation in human medicine, they look to the possibilities for plant pathogen defence. They agree with the authors about just how fundamental persulfidation might be in plant signalling, making the parallel with phosphorylation.

Read more

Journal of Experimental Botany publishes an exciting mix of research, review and comment on fundamental questions of broad interest in plant science. Regular special issues highlight key areas.

Article source: Jonathan Ingram, Journal of Experimental Botany.

Image: Persulfidated proteins in the plant glycolysis pathway. Reproduced from the paper by Aroca et al. (Open Access, see https://creativecommons.org/licenses/by/4.0/).

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